Early life adversity during the infant sensitive period for attachment: Programming of behavioral neurobiology of threat processing and social behavior
Open accessAbstract
Animals, including humans, require a highly coordinated and flexible system of social behavior and threat evaluation. However, trauma can disrupt this system, with the amygdala implicated as a mediator of these impairments in behavior. Recent evidence has further highlighted the context of infant trauma as a critical variable in determining its immediate and enduring consequences, with trauma experienced from an attachment figure, such as occurs in cases of caregiver-child maltreatment, as particularly detrimental. This review focuses on the unique role of caregiver presence during early-life trauma in programming deficits in social behavior and threat processing. Using data primarily from rodent models, we describe the interaction between trauma and attachment during a sensitive period in early life, which highlights the role of the caregiver's presence in engagement of attachment brain circuitry and suppressing threat processing by the amygdala. These data suggest that trauma experienced directly from an abusive caregiver and trauma experienced in the presence of caregiver cues produce similar neurobehavioral deficits, which are unique from those resulting from trauma alone. We go on to integrate this information into social experience throughout the lifespan, including consequences for complex scenarios, such as dominance hierarchy formation and maintenance.
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Written from the paper’s full text.
TL;DR
This review argues that early-life trauma occurring within the attachment context—abuse from a caregiver or trauma in the caregiver’s presence—during a sensitive period programs lasting deficits in threat processing and social behavior, with the amygdala as a key mediator. Rodent models show that caregiver presence engages attachment circuitry and suppresses amygdala-dependent threat learning, producing outcomes distinct from trauma alone.
Key findings
- During the rat sensitive period for attachment (PN<9), low corticosterone blocks amygdala plasticity; odor-shock conditioning instead produces odor approach/attachment learning via elevated norepinephrine and olfactory bulb/anterior piriform circuitry. After PN9, pups alone can learn amygdala-dependent fear if corticosterone rises, but the mother’s presence socially buffers the stress response and reverts pups to preference learning until about PN15.
- Abuse from the caregiver (e.g., low-bedding maternal maltreatment) or repeated odor-shock paired with maternal odor during the sensitive period produces latent amygdala-dependent deficits: decreased social exploration in adolescence, depressive- and anxiety-like behavior in adulthood, impaired threat/aversion learning, and blunted amygdala activation during fear conditioning. These effects are not produced by shock alone or unpaired odor-shock.
- Direct abuse and paired odor-shock produce indistinguishable neurobehavioral outcomes. Corticosterone injection uncovers deficits—disordered attachment, decreased approach to maternal odor, less nipple attachment, and amygdala hyperactivity—in abused or paired odor-shock pups, but not in pups reared by a nurturing mother or given shock trauma alone.
- The review proposes that early caregiver abuse may impair dominance hierarchy formation and maintenance through altered aggression, threat response, social exploration, and sexual motivation; subordinate rats in visible burrow systems show elevated corticosterone, increased illness/weight loss, reduced activity and social behavior, and increased defensive responses.
Methods
- Narrative review synthesizing rodent, nonhuman primate, and human literature, with a focus on species-atypical abusive maternal care in rodent models.
- Data primarily from rodent paradigms including odor-shock fear conditioning, low-bedding maternal abuse, maternal social buffering, and visible burrow system dominance studies; no new empirical data are reported.
- Main analysis is conceptual integration of cited findings; no systematic search strategy or quantitative synthesis is stated.
Limitations
- The paper states that translating rodent data to humans can be challenging and that future work is needed to determine whether humans engage the same neural circuitry for attachment and whether the child brain is predisposed toward odor preferences at this age.
- The paper notes that many effects of early-life trauma remain latent until peri-adolescence, making abused children difficult to identify without physical evidence; the specific time-course of the human stress hypo-responsive period is unknown, and oxytocin’s role in very early life and the attachment sensitive period remains unclear.
- Evident from the text: this is a narrative review rather than a systematic or meta-analytic synthesis, it relies heavily on rodent models, several cited findings are “in press,” and the dominance hierarchy consequences are largely proposed/putative rather than directly tested in abused animals.
Model-written summary. Check it against the paper before relying on it.
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Cites
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Claims the paper makes
0 of 167 cited sources checked · 0 supported · 0 flagged
- Findingown data
Trauma experienced in the presence of the caregiver has similar neurobehavioral consequences as trauma experienced directly from an abusive caregiver.
“In particular, we have observed that trauma experienced in the presence of the caregiver has similar neurobehavioral consequences as trauma experienced directly from an abusive caregiver; these socially anchored traumas produce unique and profound effects that go beyond those of trauma alone.”
Quote in the paperSubstantial claim - Premisecitation
Trauma experienced from an attachment figure during a sensitive window in early life can produce life-long deficits in threat processing and social behavior across many species.
“In particular, trauma experienced from a caregiver during a sensitive window in early life can produce life-long deficits in threat processing and social behavior across many species (Amaral, 2003, Callaghan et al., 2014, McEwen, 2003, Moriceau et al., 2006, Tang et al., 2014, Tzanoulinou and Sandi, 2017, Zeanah et al., 2003).”
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Soothing a stressed infant can lower stress hormone levels.
“In turn, this stimulation of the infant's sensory systems changes physiology; for example, soothing a stressed infant can lower stress hormone levels (Gunnar and Quevedo, 2007, Gunnar et al., 2007, Hofer, 1994, Sarro et al., 2014a, Sarro et al., 2014b).”
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- cites Gunnar et al., 2007
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- Premisecitation
Bowlby's Attachment Theory described the infant brain of altricial species as designed to support attachment to the caregiver, even when the quality of care is compromised or abusive, during a temporally defined sensitive period.
“Indeed, John Bowlby’s Attachment Theory described the infant brain of altricial species as designed to support attachment to the caregiver, even when the quality of care is compromised or abusive, during a temporally defined sensitive period (Bowlby, 1965, Bowlby, 1978).”
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In typically developing children, caregiver regulation of infant physiology is critical for a child's interaction with the world, including reduction of fear, response to novelty, and learning.
“In typically developing children, this caregiver regulation of infant physiology has been shown to be critical for a child’s interaction with the world, including reduction of fear, response to novelty, and learning (Humphreys and Zeanah, 2015, Gee et al., 2013, Nachmias et al., 1996).”
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- Premisecitation
Studies in rodents, primates, and humans have identified a sensitive period in early life during which abusive care from an attachment figure interacts with heightened neural plasticity to program long-term impairments in social behavior through effects on amygdala development.
“Indeed, studies in rodents, primates, and humans have identified a sensitive period in early life during which abusive care from an attachment figure interacts with heightened neural plasticity to program long-term impairments in social behavior through effects on amygdala development (Opendak and Sullivan, 2016, Humphreys and Zeanah, 2015, Drury et al., 2015).”
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Once pups are born, a novel odor placed either on the mother or in the air surrounding her will readily take on the properties of maternal odor.
“Once pups are born, a new maternal odor can be rapidly learned; a novel odor (e.g. peppermint) placed either on the mother or in the air surrounding her will readily take on the properties of maternal odor (Cheslock et al., 2000, Roth and Sullivan, 2005, Sullivan et al., 1990).”
Quote in the paperNot a substantial claim0 of 3 sources checked - Interpretationown data
Socially anchored traumas (trauma with caregiver cues and abuse) produce unique and profound effects that go beyond those of trauma alone.
“In particular, we have observed that trauma experienced in the presence of the caregiver has similar neurobehavioral consequences as trauma experienced directly from an abusive caregiver; these socially anchored traumas produce unique and profound effects that go beyond those of trauma alone.”
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Processing of trauma in early life is different from processing such information in adulthood.
“As will be shown below, processing of trauma in early life is different from processing such information in adulthood (Gunnar et al., 2007, Opendak and Sullivan, 2016, Teicher et al., 2003).”
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- cites Opendak and Sullivan, 2016
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- Premisenone given
During early life, the infant relies on the caregiver for regulation of basic physiology, ranging from vital functions, such as heart rate and respiration, to emotional regulation.
“Furthermore, during early life, the infant relies on the caregiver for regulation of basic physiology, ranging from vital functions, such as heart rate and respiration, to emotional regulation.”
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Data from children raised in institutional care typically reflects the consequences of neglect, rather than abuse.
“For instance, data from children raised in institutional care typically reflects the consequences of neglect, rather than abuse (Humphreys and Zeanah, 2015).”
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- Premisenone given
The first ten days of life represent a sensitive period for forming attachments in rats.
“As will be discussed further, these first ten days represent a sensitive period for forming attachments.”
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Abused children frequently long to be reunited with their abusive attachment figure after separation and placement in a safe home.
“This feature of attachment formation is supported by clinical and epidemiological literature indicating that abused children frequently long to be reunited with their abusive attachment figure after separation and placement in a safe home (Ainsworth, 1969, Perry and Sullivan, 2014).”
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- cites Perry and Sullivan, 2014
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Maternal odor is of paramount importance to pups' survival, as they rely on this odor cue for nipple attachment, proximity seeking, and social behavior.
“Specifically, maternal odor is of paramount importance to pups’ survival, as they rely on this odor cue for nipple attachment, proximity seeking, and social behavior.”
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The large amounts of NE required for attachment-related plasticity result from the failure of the infant LC to show habituation or to turn itself off via auto-inhibition.
“In particular, the large amounts of NE required for this attachment-related plasticity results from the failure of the infant LC to show habituation or to turn itself off via auto-inhibition (as occurs in older pups and adults) (Nakamura et al., 1987, Winzer-Serhan et al., 1996).”
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At PN10 in rodents, the SHRP begins to wane and CORT release increases in response to shock and other stressful stimuli.
“At PN10 in rodents, the SHRP begins to wane and we begin to see increases in CORT release in response to shock and other stressful stimuli in pups (Sullivan and Holman, 2010).”
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- Premisecitation
Social buffering of the infant is a dynamic process that wanes as individuals across species mature and become independent.
“Social buffering of the infant is a dynamic process that wanes as individuals across species mature and become independent (Gee et al., 2014, Levine, 2001, McCormack et al., 2009, Sanchez, 2006, Stanton and Levine, 1990, Suchecki et al., 1995, van Oers et al., 1998) (Fig. 1).”
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During the sensitive period for attachment learning (PN < 9), low CORT levels block amygdala plasticity to prevent pups from learning amygdala-dependent fear/threat.
“Data indicate that during the sensitive period for attachment learning (PN < 9), low CORT levels block amygdala plasticity to prevent pups from learning amygdala-dependent fear/threat.”
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NE levels are very high in humans at birth and over the first two years of life.
“Notably, NE levels are very high in humans at birth and over the first two years of life (Lagercrantz and Bistoletti, 1977).”
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In pups older than PN9, fear conditioning accesses the amygdala to support fear/threat learning if the pup is alone.
“In pups older than PN9, this fear conditioning paradigm accesses the amygdala to support fear/threat learning if the pup is alone.”
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There appears to be a similar stress hypo-responsive period in human children.
“Although the specific time-course is unknown, there appears to be a similar stress hypo-responsive period in human children.”
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Both natural maternal odor and a learned artificial maternal odor generate the same responses from the olfactory bulb.
“It is important to note that both natural maternal odor and a learned artificial maternal odor generate the same responses from the olfactory bulb (Raineki et al., 2010c, Roth and Sullivan, 2005).”
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The fear conditioning paradigm activates the attachment learning neural circuit involving elevated NE to produce approach responses to the odor.
“Instead, this learning paradigm activates the attachment learning neural circuit involving elevated NE (thick gray arrow) to produce approach responses to the odor (Moriceau et al., 2006).”
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A more adult-like fear learning system, which cannot be switched on/off by CORT, develops by PN15.
“A more adult-like fear learning system, which cannot be switched on/off by CORT develops by PN15.”
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The mother-controlled switch between fear and attachment learning is mediated through the mother's ability to control pups CORT.
“This mother-controlled switch between fear and attachment learning is mediated through the mother’s ability to control pups CORT (Sullivan, in press).”
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- Premisecitation
Maternal presence dampens cortisol reactivity to threats in children even when they behaviorally exhibit fear.
“This has been demonstrated in children, for whom maternal presence dampens cortisol reactivity to threats even when they behaviorally exhibit fear (Nachmias et al., 1996).”
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Infants begin to exhibit dampened cortisol reactivity during the first year of life (6-12 months).
“Studies show that infants begin to exhibit dampened cortisol reactivity during the first year of life (6–12 months) (Gunnar and Donzella, 2002, Gunnar et al., 2015).”
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Basal cortisol remains at low levels through the preschool period.
“Although the duration of this period is unknown, basal cortisol remains at low levels through the preschool period (Grunau et al., 2004, Watamura et al., 2004).”
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Abuse and repeated odor-shock generate latent changes in amygdala function emerging around weaning age.
“Although abuse and repeated odor-shock fails to produce an aversion to maternal odor, these manipulations generate latent changes in amygdala function that emerge around weaning age.”
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At PN10, the mother begins to socially buffer the stress response in a manner similar to adults.
“The mother also begins to socially buffer the stress response, in a manner similar to that seen in adults.”
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The amygdala is mature enough to support threat learning in pups as young as PN6, provided sufficient corticosterone within the amygdala.
“Indeed, the amygdala is mature enough to support threat learning in pups as young as PN6, provided sufficient levels of corticosterone are available within the amygdala (Debiec and Sullivan, 2014, Moriceau et al., 2004, Moriceau et al., 2009, Moriceau and Sullivan, 2004, Moriceau and Sullivan, 2006).”
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Maternal social buffering can reopen pups' sensitive period for attachment between PN10-15.
“This social buffering by the mother has profound effects on whether pups have access to the attachment learning neural circuitry: the maternal social buffering can reopen pups sensitive period for attachment between the ages of PN10-15.”
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The inability of the paired odor-pain procedure to produce fear learning is not due to pups' inability to detect the aversive stimulus or feel pain.
“The inability of the paired odor-pain procedure to produce fear learning is not due to pups’ inability to detect the aversive stimulus or feel pain.”
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Across many species, many effects of infant abuse remain latent until peri-adolescence.
“Across many species, many of the effects of infant abuse remain latent until peri-adolescence (Adriani and Laviola, 2004, Amaral, 2003, Andersen and Teicher, 2008, Bauman et al., 2006, Costello et al., 2003).”
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Termination of the sensitive period for attachment at PN10 in typical rearing is primarily due to increasing CORT and functional emergence of the amygdala.
“As mentioned above, termination of the sensitive period for attachment at PN10 in typical rearing conditions is primarily due to increasing levels of CORT and functional emergence of the amygdala (Sullivan and Holman, 2010).”
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Quality of care alters how well the caregiver can regulate the infant's physiology, while preserving attachment.
“The quality of care an infant receives from the caregiver, while preserving attachment, does alter how well the caregiver can regulate the infant’s physiology.”
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Increasing CORT during the sensitive period can prematurely end sensitive period learning.
“Specifically, increasing CORT during the sensitive period, either via rearing with an abusive mother, or through pharmaceutical manipulations (systemic injections or by intra-amygdala microinfusions), can prematurely end sensitive period learning.”
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Highly stressed caregivers have a reduced capacity to socially buffer children.
“For instance, highly stressed caregivers have a reduced capacity to socially buffer children (Ainsworth and Bell, 1970, Gunnar et al., 2007, Gunnar et al., 1996, Nachmias et al., 1996).”
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Direct abuse from the caregiver and pairing of the maternal odor with shock produce indistinguishable neurobehavioral outcomes.
“Importantly, direct abuse from the caregiver and pairing of the maternal odor with shock produce indistinguishable neurobehavioral outcomes.”
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Traumatic cues during the sensitive period for attachment are processed within the attachment circuitry rather than the threat processing circuitry.
“Due to the unique neurobiology of the infant brain that is biased towards forming attachments, traumatic cues during the sensitive period for attachment are processed within the attachment circuitry rather than the threat processing circuitry.”
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In infant rodents, social buffering by the mother attenuates stress hormone release by the HPA axis at the PVN through suppression of NE afferents from medullary A1/A2 noradrenergic neurons.
“It has been shown that in infant rodents, social buffering by the mother greatly attenuates stress hormone release by the HPA axis at the level of the hypothalamic paraventricular nucleus (PVN), through suppression of NE afferents from medullary A1/A2 noradrenergic neurons (Shionoya et al., 2007)–a system identified in adults (Ziegler and Herman, 2002).”
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Throughout the animal kingdom, young, including humans, form attachments to abusive caregivers.
“In spite of this, throughout the animal kingdom, young, including humans, form attachments to abusive caregivers (Harlow and Harlow, 1965, Hess, 1962, Rajecki et al., 1978, Salzen, 1970, Stanley, 1962).”
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Many effects of early life trauma on children's mental health appear delayed until transition into adolescence.
“In parallel with observations of latent abuse-related deficits in rodents and non-human primates, many of the effects of early life trauma on children’s mental health appear to be delayed until they begin to transition into adolescence (Bachevalier and Loveland, 2006, Bachevalier et al., 2001, Callaghan et al., 2014, Goursaud and Bachevalier, 2007, Goursaud et al., 2014, Machado and Bachevalier, 2”
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Caregiver abuse decreases sexual motivation in adult rodents.
“Furthermore, caregiver abuse decreases sexual motivation in adult rodents (Raineki et al., 2015), suggesting that these animals may fail to engage receptive females, a benefit of dominance in typically-reared individuals (Blanchard et al., 1995, Blanchard et al., 1988, White et al., 1986).”
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Adult monkeys without amygdalae display inappropriate social behavior.
“Moreover, studies in nonhuman primates demonstrate that adult monkeys without amygdalae display inappropriate social behavior (Amaral, 2003, Baron-Cohen et al., 2000, Bliss-Moreau et al., 2011, Brothers et al., 1990, Emery et al., 2001, Malkova et al., 2010).”
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In rat pups, social behavior deficits and heightened amygdala neural activity can be uncovered only during periods of heightened stress combined with early life trauma.
“It is important to note that while social behavior in adult rats involves the amygdala and can be a behavioral measure used to reveal those adults with early life trauma, in rat pups, it is only during periods of heightened stress (eg. heightened CORT levels) combined with early life trauma that social behavior deficits and heightened amygdala neural activity can be uncovered.”
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Stress can uncover deficits associated with trauma that may otherwise be hidden.
“However, stress can uncover deficits associated with trauma that may otherwise be hidden, as demonstrated by Mary Ainsworth’s Strange Situation Test.”
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Compromised amygdala function in animals with history of caregiver abuse during sensitive period may have highly maladaptive consequences for social position.
“Compromised amygdala function in animals with a history of caregiver abuse during the sensitive period for attachment may have highly maladaptive consequences with respect to social position (Fig. 3).”
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Social behavior in adult rodents appears to rely on the medial amygdala.
“Social behavior in adult rodents appears to rely on the medial amygdala (Rasia-Filho et al., 2000).”
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In the visible burrow system, rats rapidly form stable dominance hierarchies.
“This can be simulated in the laboratory using a visible burrow system, a semi-naturalistic enclosure that replicates many of the challenges and opportunities of group-living in nature; in this setting, rats rapidly form stable dominance hierarchies (Fig. 3) (Blanchard et al., 1995, Blanchard et al., 1988, Opendak et al., 2016).”
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Aberrant processing of social and threatening cues from amygdala dysfunction is a hallmark of psychiatric sequelae following early-life abuse/neglect.
“Aberrant processing of social and threatening cues stemming from amygdala dysfunction is a hallmark of psychiatric sequelae following early-life abuse and neglect (Levin et al., 2015, Teicher et al., 2003, Troller-Renfree et al., 2016, Zeanah and Gleason, 2015).”
Quote in the paperSubstantial claim0 of 3 sources checked - Interpretationcitation
Attachments formed in threatening/traumatic contexts have unique consequences for development of social behavior and threat learning.
“However, attachments formed in threatening or traumatic contexts have unique consequences for the development of social behavior and learning about threat.”
Quote in the paperSubstantial claim - Interpretationreasoning
Abuse may affect formation and maintenance of a stable dominance hierarchy.
“As a result, abuse may affect formation and maintenance of a stable dominance hierarchy.”
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In the clinical population, the amygdala has been implicated in the pathogenesis of psychiatric sequelae.
“In the clinical population, the amygdala has also been implicated in the pathogenesis of psychiatric sequelae.”
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Caregiver abuse during the sensitive period for attachment produces a unique outcome, with the social dimension of early abuse, rather than pain alone, predisposing amygdala development towards an impaired phenotype.
“These results suggest that caregiver abuse during the sensitive period for attachment produces a unique outcome, with the social dimension of early abuse, rather than pain alone, predisposing amygdala development towards an impaired phenotype.”
Quote in the paperSubstantial claim- Rests on an assumption: Rough handling by the mother given low nesting resources and repeated presentations of paired odor-shock during the sensitive period for attachment are valid models of caregiver abuse in rodents.
- Premisecitation
The effects of rough handling and paired odor-shock are not produced when a pup experiences shock without the mother.
“Importantly, these effects are not produced when a pup experiences shock without the mother (Sarro et al., 2014a, Tyler et al., 2007).”
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PremisecitationHippocampus-dependent contextual fear learning emerges around postnatal day 23 in rodents.
“For instance, hippocampus-dependent contextual fear learning emerges around postnatal (PN) day 23 in rodents (Raineki et al., 2010a), while other hippocampal dependent learning behaviors emerge either before or after this age (Moye and Rudy, 1987, Stanton, 2000).”
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PremisecitationIn rat pups, learning of maternal odor begins in the prenatal environment, where amniotic odors can guide nipple attachment as soon as pups are born.
“In rat pups, this learning process begins in the prenatal environment, where amniotic odors can guide nipple attachment as soon as pups are born.”
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PremisecitationThe amygdala and hippocampus become functionally mature in normal rearing conditions at PN10 and PN23, respectively.
“Evidence from rodent studies on development of the amygdala and hippocampus show a similar developmental time course; both regions demonstrate considerable growth during the initial postnatal period and become functionally mature in normal rearing conditions at PN10 and PN23, respectively (Chareyron et al., 2012b, Raineki et al., 2010a, Raineki et al., 2010c).”
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- cites Raineki et al., 2010a
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- cites Raineki et al., 2010c
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PremisecitationThe amygdala is the critical structure involved in the formation and storage of conditioned fear associations, but it also has a role in many emotional functions including social odor processing and assessing hedonic value of stimuli.
“The amygdala is considered to be the critical structure involved in the formation and storage of conditioned fear associations (Davis et al., 1994, Phelps and LeDoux, 2005), but it has a role in many emotional functions, including those unrelated to fear, such as social odor processing and assessing hedonic value of stimuli (Holland and Gallagher, 2004, Maren and Fanselow, 1996, Phelps and LeDoux,”
Quote in the paperNot a substantial claim0 of 3 sources checkedProbably not a substantial claim: may not pass S4 (based).
Premisenone givenAttachment to a caregiver during a sensitive window is of paramount importance to altricial infant survival due to the infant's greatly reduced ability to acquire food, protection, and warmth.
“Attachment to a caregiver during a sensitive window is of paramount importance to altricial infant survival due to the infant’s greatly reduced ability to acquire food, protection, and warmth.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationNeonatal amygdala connectivity correlates with fear responses at six months of age in human infants.
“It has been suggested that neonatal amygdala connectivity correlates with fear responses at six months of age in human infants (Graham et al., 2016).”
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PremisecitationPups without the ability to smell rarely survive as they frequently fail to nipple attach and can become malnourished.
“Indeed, pups without the ability to smell rarely survive as they frequently fail to nipple attach and can become malnourished (Landers and Sullivan, 2012).”
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PremisecitationThe amygdala-hippocampus-PFC circuit is crucial for threat detection and many forms of social behavior, but the maturation and connectivity between these brain regions develops slowly over early life in humans, nonhuman primates, and rodents.
“The amygdala-hippocampus-PFC circuit is crucial for threat detection and many forms of social behavior, but the maturation and connectivity between these brain regions develops slowly over early life in humans (Casey et al., 2005, Gee et al., 2013, Graham et al., 1999, Malter Cohen et al., 2013, Skuse et al., 2003, Tottenham, 2012, Tottenham and Sheridan, 2009), nonhuman primates (Bachevalier and”
Quote in the paperSubstantial claim0 of 3 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationAmygdala volume peaks in pre-adolescence.
“Furthermore, volumetric analysis indicates that amygdala volume peaks in pre-adolescence (Uematsu et al., 2012).”
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PremisecitationA neutral odor can acquire the valence of a maternal odor if placed into the amniotic fluid a few days before birth, suggesting the odor itself is arbitrary for both rats and mice.
“Even a neutral odor can acquire the valence of a maternal odor if placed into the amniotic fluid a few days before birth, suggesting the odor itself is arbitrary for both rats and mice (Hepper and Cleland, 1998, Leon, 1992, Logan et al., 2012, Pedersen and Blass, 1982, Smotherman and Robinson, 1987, Sullivan and Leon, 1986, Sullivan and Wilson, 1991).”
Quote in the paperNot a substantial claim0 of 3 sources checkedMay combine two claims.
PremisecitationDuring the first ten days of life, learning-associated plasticity for new maternal odors in rat pups occurs within the olfactory bulb and requires an odor paired with copious amounts of NE.
“During the first ten days of life, the learning process for new maternal odors in rat pups occurs through a relatively simple neurobiological substrate. At this early age, learning-associated plasticity occurs within the olfactory bulb, the first relay station for olfactory processing. This process requires that an odor is paired with copious amounts of NE (Sullivan et al., 2000b, Sullivan et al.,”
Quote in the paperNot a substantial claim0 of 3 sources checkedMay combine two claims.
PremisereasoningThe sole source of NE to the olfactory bulb is the LC, and this structure's unique physiology during early life is essential for neonatal odor approach learning.
“The sole source of the NE to the olfactory bulb is the LC, and this structure’s unique physiology during early life is essential for neonatal odor approach learning.”
Quote in the paperNot a substantial claimMay combine two claims.
Premisenone givenShock induces activation of the HPA axis and CORT release, which is necessary for the young amygdala to learn.
“A critical feature of this learning is that shock induces activation of the HPA axis and CORT release, which is necessary for the young amygdala to learn.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationSocial buffering describes the reduction of both the stress response and release of stress hormones, and has been observed in myriad species and throughout the lifespan.
“Social buffering is a phenomenon that has been observed in myriad species and throughout the lifespan and describes the reduction of both the stress response and release of stress hormones (Ditzen and Heinrichs, 2014, Hennessy et al., 2009, Hostinar et al., 2015, Kikusui et al., 2006, Sanchez et al., 2015, Sullivan and Perry, 2015, Takahashi et al., 2013).”
Quote in the paperNot a substantial claim0 of 3 sources checkedMay combine two claims.
PremisecitationHuman infants show learning of caregiver cues across multiple sensory modalities, enabling them to form attachments to adoptive parents and caregivers of either sex.
“Human infants also show learning of caregiver cues across multiple sensory modalities (DeCasper and Fifer, 1980, Sullivan et al., 2011), which enables them to form attachments to adoptive parents and caregivers of either sex.”
Quote in the paperNot a substantial claim0 of 2 sources checkedMay combine two claims.
PremisereasoningThe sensitive period terminates when pups are around 10 days old, as the LC becomes more adult-like: NE release is greatly restricted due to development of recurrent collaterals that quickly self-inhibit the LC's response.
“The sensitive period terminates when pups are around 10 days old, as the LC becomes more adult-like: NE release is greatly restricted due to the development of recurrent collaterals that quickly self-inhibit the LC’s response.”
Quote in the paperSubstantial claimMay combine two claims.
PremisecitationAt birth, rat pups have a functional HPA axis that soon becomes hypo-responsive and not activated by most painful stimuli, a period termed the stress hypo-responsive period (SHRP).
“For example, at birth, rat pups have a functional HPA axis, although it soon becomes hypo-responsive and not activated by most painful stimuli, a period of life termed the stress hypo-responsive period (SHRP) (Dallman, 2000, Stanton and Levine, 1985).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Dallman, 2000 source
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- cites Stanton and Levine, 1985
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PremisereasoningThe odor takes on qualities of the maternal odor to support nipple attachment and enhance prosocial behaviors to the mother.
“The odor also takes on qualities of the maternal odor to support nipple attachment and enhance prosocial behaviors to the mother.”
Quote in the paperNot a substantial claimMay combine two claims.
PremisecitationNE plays a critical role in bond formation in numerous species, suggesting it is a phylogenetically conserved system.
“Although it remains unclear whether learning in human infants is the same as the rodent, NE plays a critical role in bond formation in numerous species (Nelson and Panksepp, 1998, Numan and Young, 2016), suggesting it is a phylogenetically conserved system.”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites Nelson and Panksepp, 1998
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- cites Numan and Young, 2016 source
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PremisereasoningIf the mother is present, she socially buffers the pup's stress response, and pups revert to sensitive period learning and learn an odor preference.
“However, if the mother is present, she socially buffers the pup’s stress response, and pups revert to sensitive period learning and learn an odor preference (red dashed line).”
Quote in the paperSubstantial claimMay combine two claims.
PremisecitationThe anterior piriform is activated by odors learned during the sensitive period, while the posterior piriform is engaged in response to learned odor in older pups and adults.
“In particular, the anterior piriform is activated by odors learned during this sensitive period, while the posterior piriform is engaged in response to learned odor in older pups and adults (Moriceau and Sullivan, 2006, Moriceau et al., 2006, Roth and Sullivan, 2005).”
Quote in the paperNot a substantial claim0 of 3 sources checked- cites Moriceau and Sullivan, 2006
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- cites Moriceau et al., 2006
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- cites Roth and Sullivan, 2005 source
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Premisenone givenEarly infants learn attachment regardless of quality of care; older infants (PN10-PN15) learn fear when away from mother or attachment if with mother.
“Early infants will learn attachment regardless of the quality of care, while slightly older infants (PN10-PN15) will either learn to fear a traumatic associated stimulus when away from the mother or learn an attachment if acquisition takes place with the mother.”
Quote in the paperSubstantial claimMay combine two claims.
PremisecitationOnly early life trauma associated with attachment leads to lifelong amygdala-dependent behavioral deficits, such as poor social behavior (onset prior to weaning) and depressive-like behaviors (onset post-weaning).
“Testing later in life shows that only the early life trauma associated with attachment will lead to lifelong amygdala-dependent behavioral deficits, such as poor social behavior (onset prior to weaning) and depressive-like behaviors (onset post- weaning (Raineki et al., 2012, Raineki et al., 2010b, Sevelinges et al., 2011, Sullivan et al., 2000a, Sullivan et al., 2000b).”
Quote in the paperSubstantial claim0 of 3 sources checkedMay combine two claims.
PremisecitationIn adulthood, early trauma produces enhanced aggression and impaired threat response.
“In adulthood, early trauma produces enhanced aggression (Marquez et al., 2013) and impaired threat response (Perry, in press).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Marquez et al., 2013 source
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- cites Perry, in press
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May combine two claims.
PremisecitationPairing painful maternal care with a novel peppermint odor does not activate the survival circuit for aversion learning; instead pups learn to approach the odor, which takes on qualities of maternal odor.
“Pairing this painful maternal care with a novel peppermint odor does not activate the important survival circuit within the brain to support aversion learning. Rather, pups not only learn to approach this odor, but this odor takes on the qualities of maternal odor to support nipple attachment and prosocial behaviors (Roth and Sullivan, 2005, Sullivan et al., 1986, Sullivan et al., 2000a).”
Quote in the paperSubstantial claim0 of 3 sources checked- cites Roth and Sullivan, 2005 source
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- cites Sullivan et al., 1986
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- cites Sullivan et al., 2000a
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PremisecitationPups reared by an abusive mother during the SHRP receive CORT through her milk and her social buffering is compromised; when trained on peppermint odor-shock outside the nest at PN7, they learn an aversion through amygdala-dependent mechanisms.
“Pups reared by an abusive mother during the SHRP receive CORT through her milk and her ability to socially buffer this CORT elevation is compromised; when these pups are trained on a peppermint odor-shock conditioning paradigm outside the nest at PN7, they will learn an aversion through amygdala-dependent mechanisms (Moriceau et al., 2004, Raineki et al., 2010b).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Moriceau et al., 2004
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- cites Raineki et al., 2010b
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PremisecitationAt PN10, stressful stimuli produce a more immediate increase in pups' CORT levels, and the presence of the mother completely blocks its release.
“Specifically, at PN10, stressful stimuli begin to produce a more immediate increase in pups’ CORT levels, and the presence of the mother completely blocks its release (Moriceau et al., 2006, Stanton and Levine, 1990, Suchecki et al., 1993).”
Quote in the paperSubstantial claim0 of 3 sources checked- cites Moriceau et al., 2006
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- cites Stanton and Levine, 1990
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- cites Suchecki et al., 1993 source
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PremisecitationDuring the transitional sensitive period, maternal presence modulates whether pups learn to avoid or prefer an odor paired with shock; this process depends on amygdala serotonin and CORT levels.
“In particular, during this transitional sensitive period, maternal presence can modulate whether pups learn to avoid or prefer an odor paired with shock; this process depends on amygdala serotonin and CORT levels (Moriceau et al., 2006) (Fig. 2).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Moriceau et al., 2006
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PremisecitationAmygdala-dependent deficits are task-specific: amygdala hyperactivity underlies decreased social exploration in adolescence and depressive/anxiety-like behavior in adulthood, in parallel with impaired threat aversion learning and blunted amygdala activation during fear conditioning.
“Amygdala-dependent deficits are expressed in a task-specific manner: amygdala hyperactivity underlies decreased social exploration in adolescence and depressive and anxiety-like behavior in adulthood (Fig. 2), in parallel with impaired ability to learn aversions to threat and blunted amygdala activation during fear conditioning (Raineki et al., 2012, Sevelinges et al., 2007, Sevelinges et al., 201”
Quote in the paperSubstantial claim0 of 3 sources checkedMay combine two claims.
PremisecitationPairing an odor with a moderately painful foot-shock (0.5 mA) or tail-pinch produces an odor preference in young pups; the procedure also produces a new maternal odor that pups prefer.
“Just as new maternal odors can be learned when a previously neutral odor is paired with stimuli evoking maternal care, such as milk or stroking, we paired an odor with a moderately painful foot-shock (0.5 mA) or tail-pinch; this produced an odor preference in young pups (Camp and Rudy, 1988, Haroutunian and Campbell, 1979, Spear, 1978, Sullivan et al., 1986); we later showed this procedure also”
Quote in the paperSubstantial claim0 of 3 sources checked- cites Camp and Rudy, 1988
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- cites Haroutunian and Campbell, 1979
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- cites Spear, 1978
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Premisenone givenAbused pups or pups injected with CORT can learn arbitrary odor aversions via premature amygdala engagement, but always show a preference for the maternal odor.
“It is important to note that, although abused pups or pups injected with CORT can learn arbitrary odor aversions (eg. peppermint) via premature amygdala engagement, they will nevertheless always show a preference for the maternal odor.”
Quote in the paperSubstantial claimMay combine two claims.
PremisecitationBoth rough handling by the mother given low nesting resources and repeated presentations of paired odor-shock during the sensitive period for attachment produce latent changes in amygdala function.
“Both of these manipulations produces latent changes in amygdala function and depressive-like behavior, aberrant fear expression, and social behavior deficits (Perry et al., in press; Raineki et al., 2010b, Raineki et al., 2010c, Raineki et al., 2015, Roth et al., 2014, Sevelinges et al., 2007, Sevelinges et al., 2011, Sevelinges et al., 2008).”
Quote in the paperSubstantial claim0 of 3 sources checked- cites Perry et al., in press
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- cites Raineki et al., 2010b
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- cites Raineki et al., 2010c
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- Rests on an assumption: Rough handling by the mother given low nesting resources and repeated presentations of paired odor-shock during the sensitive period for attachment are valid models of caregiver abuse in rodents.
May combine two claims.
PremisecitationRats with history of caregiver abuse show impaired response to predator odor threat and amygdala dysfunction.
“Rats with a history of caregiver abuse show impaired response to a salient predator odor threat and amygdala dysfunction, suggesting that maintenance of a social hierarchy may also be compromised in these animals (Perry et al., in press) (Fig. 3).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Perry et al., in press
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PremisecitationDominant rats show enhanced adult neurogenesis in the ventral dentate gyrus; effect also shown in baboons.
“Specifically, dominant rats show enhanced adult neurogenesis in the ventral dentate gyrus of the hippocampal formation, an effect that also has been shown in baboons (Kozorovitskiy and Gould, 2004, Peragine et al., 2014, Wu et al., 2014).”
Quote in the paperNot a substantial claim0 of 3 sources checked- cites Kozorovitskiy and Gould, 2004
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- cites Peragine et al., 2014 source
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- cites Wu et al., 2014
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InterpretationreasoningEarly life provides a sensitive window for programming lifelong emotional and cognitive processing, influencing threat-processing and social behaviors.
“Early life provides a sensitive window for programming lifelong emotional and cognitive processing, which has profound influence over threat-processing and social behaviors.”
Quote in the paperSubstantial claimMay combine two claims.
PremisecitationAnimal models across a variety of species have allowed assessment of the mechanisms by which caregiver abuse engenders neurobehavioral deficits, with programming of the stress system as a point of convergence in adult outcomes.
“Animal models across a variety of species have allowed us to assess the mechanisms by which caregiver abuse engenders neurobehavioral deficits, with programming of the stress system as a point of convergence in adult outcomes (Andersen and Teicher, 2008, Denenberg, 1963, Famularo et al., 1992, Harlow and Harlow, 1965, Hofer, 1994, Levine, 1957, Levine et al., 1985, Teicher et al., 2003).”
Quote in the paperSubstantial claim0 of 3 sources checkedMay combine two claims.
PremisecitationIn non-human primates, infant amygdala lesions lead to decreased fear response to normally threatening stimuli and enhanced response to novel social situations.
“The most dramatic developmental differences were first observed in non-human primates, where infant amygdala lesions lead to decreased fear response to normally threatening stimuli and an enhanced response to novel social situations (Amaral, 2002, Amaral, 2003).”
Quote in the paperNot a substantial claim0 of 2 sources checkedMay combine two claims.
PremisecitationIn LE rats in laboratory enclosure, subordinate rats have elevated CORT compared to dominants and can be prone to illness and weight loss due to chronic stress.
“When LE rats form a dominance hierarchy within a laboratory enclosure, it has been shown that subordinate rats have elevated levels of CORT compared to dominants and can be prone to illness and weight loss due to chronic stress (Blanchard et al., 1995, Hardy et al., 2002).”
Quote in the paperNot a substantial claim0 of 2 sources checkedMay combine two claims.
PremisecitationIn humans, the amygdala is implicated in social behavior in adults and during development.
“In humans, the amygdala is implicated in social behavior in adults (Thomas et al., 2001), as well as during development (Skuse et al., 2003, Tottenham and Sheridan, 2009).”
Quote in the paperSubstantial claim0 of 3 sources checkedMay combine two claims.
PremisecitationIndividuals with history of abuse or disordered attachment exhibit compromised fear and social behavior, and vulnerability to later-life mental health disorders.
“In the clinical literature, this has been demonstrated in individuals with a history of abuse or disordered attachment who exhibit compromised fear and social behavior, as well as vulnerability to later-life mental health disorders (Bowlby, 1984, Bremner, 2003, Famularo et al., 1992, Graham et al., 1999, Nemeroff and Vale, 2005, Pechtel et al., 2014).”
Quote in the paperSubstantial claim0 of 3 sources checkedMay combine two claims.
InterpretationreasoningRepeatedly experiencing trauma associated with caregiver cues during the sensitive period has a unique neural signature, producing latent changes in amygdala function to program emotionality and social behavior throughout the lifespan.
“Taken together, these findings suggest that repeatedly experiencing trauma associated with caregiver cues during the sensitive period for attachment has a unique neural signature, producing latent changes in amygdala function to program emotionality and social behavior throughout the lifespan.”
Quote in the paperSubstantial claimMay combine two claims.
PremisecitationCaregiver abuse in early life produces enhanced aggression, impaired threat response, depressive/anxiety-like behavior, and decreased social exploration.
“These factors may be compromised in cases of caregiver abuse in early life, which produces enhanced aggression (Marquez et al., 2013), impaired threat response (Perry, in press), depressive and anxiety-like behavior (Raineki et al., 2012, Raineki et al., 2015 and decreased social exploration (Raineki et al., 2015).”
Quote in the paperSubstantial claim0 of 3 sources checkedMay combine two claims.
InterpretationreasoningThe amygdala is not involved with social behavior in infancy; its activation can impair social behavior at this age.
“This suggests that the amygdala is not involved with social behavior in infancy and its activation can, in fact, impair social behavior at this age.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Premisenone givenDominance hierarchies are complex social arrangements determined by individual differences that can result from early life experience.
“Dominance hierarchies provide one example of a complex social arrangement determined by individual differences that can result from early life experience.”
Quote in the paperNot a substantial claimMay combine two claims.
PremisecitationPups exposed to abuse in the low bedding procedure and repeated odor-shock pairings form a disordered attachment to the mother, expressed in decreased approach to maternal odor, less nipple attachment, and amygdala hyperactivity if given CORT injections before testing.
“This can also be modeled in rodents: pups that were exposed to abuse in the low bedding procedure and repeated odor-shock pairings form a disordered attachment to the mother, expressed in decreased approach behavior towards the maternal odor, less nipple attachment, and amygdala hyperactivity if given CORT injections before testing (Raineki et al., 2012).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Raineki et al., 2012 source
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InterpretationreasoningEarly life may be a period of rapid change and heightened vulnerability of the amygdala to environmental influence, as well as multiple interconnected brain regions, including the hippocampus and PFC.
“This suggests that early life may be a period of rapid change and, likewise, heightened vulnerability of the amygdala to environmental influence, as well as multiple interconnected brain regions, including the hippocampus and PFC (Ehrlich and Josselyn, 2016, Ehrlich et al., 2012, Lupien et al., 2009).”
Quote in the paperSubstantial claim0 of 3 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationPatients with depression show alterations in amygdala function and its connectivity with other brain areas.
“For instance, patients with depression also show alterations in amygdala function and its connectivity with other brain areas (Elzinga et al., 2003, Frijling et al., 2016, Jedd et al., 2015, McEwen, 2003, Ressler and Mayberg, 2007, Savitz and Drevets, 2009, Sibille et al., 2009, Teicher et al., 2003).”
Quote in the paperNot a substantial claim0 of 3 sources checkedMay combine two claims.
PremisecitationBoth rough handling by the mother given low nesting resources and repeated presentations of paired odor-shock during the sensitive period for attachment produce social behavior deficits.
“Both of these manipulations produces latent changes in amygdala function and depressive-like behavior, aberrant fear expression, and social behavior deficits (Perry et al., in press; Raineki et al., 2010b, Raineki et al., 2010c, Raineki et al., 2015, Roth et al., 2014, Sevelinges et al., 2007, Sevelinges et al., 2011, Sevelinges et al., 2008).”
Quote in the paperSubstantial claim0 of 3 sources checked- cites Perry et al., in press
Not checked in the free run.
- cites Raineki et al., 2010b
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- cites Raineki et al., 2010c
Not checked in the free run.
- Rests on an assumption: Rough handling by the mother given low nesting resources and repeated presentations of paired odor-shock during the sensitive period for attachment are valid models of caregiver abuse in rodents.
May combine two claims.
PremisecitationBoth rough handling by the mother given low nesting resources and repeated presentations of paired odor-shock during the sensitive period for attachment produce aberrant fear expression.
“Both of these manipulations produces latent changes in amygdala function and depressive-like behavior, aberrant fear expression, and social behavior deficits (Perry et al., in press; Raineki et al., 2010b, Raineki et al., 2010c, Raineki et al., 2015, Roth et al., 2014, Sevelinges et al., 2007, Sevelinges et al., 2011, Sevelinges et al., 2008).”
Quote in the paperSubstantial claim0 of 3 sources checked- cites Perry et al., in press
Not checked in the free run.
- cites Raineki et al., 2010b
Not checked in the free run.
- cites Raineki et al., 2010c
Not checked in the free run.
- Rests on an assumption: Rough handling by the mother given low nesting resources and repeated presentations of paired odor-shock during the sensitive period for attachment are valid models of caregiver abuse in rodents.
May combine two claims.
PremisecitationBoth rough handling by the mother given low nesting resources and repeated presentations of paired odor-shock during the sensitive period for attachment produce depressive-like behavior.
“Both of these manipulations produces latent changes in amygdala function and depressive-like behavior, aberrant fear expression, and social behavior deficits (Perry et al., in press; Raineki et al., 2010b, Raineki et al., 2010c, Raineki et al., 2015, Roth et al., 2014, Sevelinges et al., 2007, Sevelinges et al., 2011, Sevelinges et al., 2008).”
Quote in the paperSubstantial claim0 of 3 sources checked- cites Perry et al., in press
Not checked in the free run.
- cites Raineki et al., 2010b
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- cites Raineki et al., 2010c
Not checked in the free run.
- Rests on an assumption: Rough handling by the mother given low nesting resources and repeated presentations of paired odor-shock during the sensitive period for attachment are valid models of caregiver abuse in rodents.
Classified as probably not a substantial claim. May combine two claims.
InterpretationreasoningEarly life is not only a sensitive period for rodent amygdala development, but also for humans.
“In light of the relationship between attachment, the amygdala, and long-term mental health outcomes, we may predict that early life is not only a sensitive period for rodent amygdala development, but also for humans.”
Quote in the paperSubstantial claimMay combine two claims.
PremisecitationThe amygdala undergoes major development progress throughout the first seven years of life in children but continues to develop into adolescence.
“The amygdala undergoes major development progress throughout the first seven years of life in children but continues to develop into adolescence (Giedd et al., 1996, Humphrey, 1968, Letcher et al., 2009, Lupien et al., 2009, Tottenham and Sheridan, 2009, Uematsu et al., 2012, Ulfig et al., 2003).”
Quote in the paperSubstantial claim0 of 3 sources checked
The paper relies on this without support.
The rodent model of abusive attachment is valid for understanding human attachment trauma.
“Due to the unique neurobiology of the infant brain that is biased towards forming attachments, traumatic cues during the sensitive period for attachment are processed within the attachment circuitry rather than the threat processing circuitry.”
The authors state this as an assumption.
The CORT injection in pups models a high-stress environment.
“The CORT injection in pups models a high-stress environment, which appears necessary to uncover neurobehavioral deficits before weaning.”
The paper relies on this without support.
Rough handling by the mother given low nesting resources and repeated presentations of paired odor-shock during the sensitive period for attachment are valid models of caregiver abuse in rodents.
“Here we have focused on two very selective models of caregiver abuse in rodents, namely, rough handling by the mother given low nesting resources, and repeated presentations of paired odor-shock during the sensitive period for attachment.”
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In primates, including humans, non-biological parents can learn to care for children after instruction or observation of experienced caretakers and infants.
“In primates, including humans, non-biological parents can learn to care for children after instruction or observation of experienced caretakers and infants1–8.”
From Oxytocin neurons enable social transmission of maternal behaviour (2021) · cites this paper as [4]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
Each contradiction between two passages listed here was confirmed by an independent check.
Sensitive-period boundary differs at PN9
MinorThe figure defines the attachment-learning sensitive period as PN < 9, excluding PN9. The text describes PN0-PN9 as the first ten days and says those ten days constitute the sensitive period.
“Data indicate that during the sensitive period for attachment learning (PN < 9), low CORT levels block amygdala plasticity to prevent pups from learning amygdala-dependent fear/threat.”
“while PN0-PN9 is thought to represent infancy (Andersen, 2003, Sullivan and Holman, 2010). As will be discussed further, these first ten days represent a sensitive period for forming attachments.”
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<scp>O</scp>xytocin modulation of neural circuits for social behavior
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Oxytocin neurons enable social transmission of maternal behaviour
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Self-citationEarly Life Trauma Has Lifelong Consequences for Sleep And Behavior
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Self-citationSocial buffering of stress – Physiological and ethological perspectives
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Self-citationDefining immediate effects of sensitive periods on infant neurobehavioral function
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Pre-adolescent stress disrupts adult, but not adolescent, safety learning
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A sensitive period for the development of episodic-like memory in mice
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Elizabeth Hamilton's Scottish Associationism: Early Nineteenth-Century Philosophy of Mind
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Toward an animal model of borderline personality disorder
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Infant Attachment and Social Modification of Stress Neurobiology
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How Our Caregivers Shape Who We Are: The Seven Dimensions of Attachment at the Core of Personality
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Attachment security and striatal functional connectivity in typically developing children
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Effects of childhood trauma on pain‐related distress in adults
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- Authors
- Opendak, M., Gould, E., & Sullivan, R.
- Affiliations
- Nathan Kline Institute for Psychiatric Research (US)
- Princeton University (US)
- Corresponding author
- Opendak, Maya
- Venue
- Developmental Cognitive Neuroscience
- Publisher
- Elsevier BV
- Published
- 2017-06
- Volume
- 25
- Pages
- 145-159
- ISSN
- 1878-9293 (ISSN-L)
- PMC
- PMC5478471
- OpenAlex
- W2587922926
- Semantic Scholar
- 108ccee8efde43db39190e144c25d4ea559dd88d
- Cited by
- 94
- References
- 305
- Citations by year
- 2026: 6 · 2025: 10 · 2024: 12 · 2023: 12 · 2022: 11 · 2021: 17 · 2020: 7 · 2019: 14 · 2018: 1 · 2017: 3
- FWCI
- 1.05
- Type
- journal article
- Language
- en
- Update notices
- erratum (2020-10-01)
- Open access
- gold
- doi.org
- Licence
- Locations
- Developmental Cognitive Neuroscience (publishedVersion, cc-by-nc-nd)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- National Institute of Mental Health (R01MH091451, F32MH112232, T32MH019524)
- National Institute on Deafness and Other Communication Disorders (R01DC009910)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R37HD083217)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Social Sciences › Psychology › Clinical Psychology › Child Abuse and Trauma
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- childhood adversity, attachment, threat processing, social behavior, amygdala, caregiver presence, trauma, dominance hierarchy, rodent models, psychobiology
- MeSH terms
- Amygdala, Animals, Brain, Child, Humans, Infant, Social Behavior, Caregivers
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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